Integrative and Comparative Biology

Integrative and Comparative Biology, volume 52, number 6, pp. 724736

doi:10.1093/icb/ics062

Society for Integrative and Comparative Biology

SYMPOSIUM

Twenty-Four Years in the Mud: What Have We Learned About

the Natural History and Ecology of the Mangrove Rivulus,
Kryptolebias marmoratus?
Brevard County Environmentally Endangered Lands Program, 91 East Drive, Melbourne, FL 32904, USA
From the symposium Mangrove Killifish: An Exemplar of Integrative Biology presented at the annual meeting of the
Society for Integrative and Comparative Biology, January 37, 2012 at Charleston, South Carolina.
1

E-mail: scott.taylor@brevardparks.com

Synopsis Although first described in 1880, Kryptolebias marmoratus avoided scientific scrutiny until 1961, when it was
identified as the only known selfing hermaphroditic vertebrate. The subsequent intense interest in this fish as a laboratory
animal, continuing to this day, might explain the paucity of wild collections, but our collective knowledge now suggests
that the inherent difficulty of wild collection is more a matter of looking in all the wrong places. Long thought to be
rare in the mangroves, and it is rare in certain human-impacted habitats, K. marmoratus can be quite abundant, but in
microhabitats not typically targeted by ichthyologists: ephemeral pools at higher elevations in the swamp, crab burrows,
and other fossorial or even terrestrial haunts. Field studies of this enigmatic fish have revealed almost amphibious
behaviors. During emersion these fish tolerate extended dry periods. In water, they are exposed to temperature extremes,
high levels of hydrogen sulfide, and depleted dissolved oxygen. Finally, their catholic diet and a geographically variable sex
life completes a portrait of an unusual animal. A clearer picture is emerging of adult life, with initial population density
estimates now known and some indication of high population turnover in burrows, but juvenile habitat and adult
oviposition sites remain unknown.

Range and nomenclature

The neotropical cyprinodontid fish, mangrove
rivulus (Kryptolebias marmoratus) has an astounding
geographical range, in fact the widest distribution of
any inshore-dwelling coastal fish species in all of
North, Central, and South Americaabout 528
of latitude and 918 of longitude (assuming that
K. marmoratus and K. ocellatus are synonomized as
per some authors). This basically encompasses the
entire tropical and subtropical eastern Atlantic
basin (Huber 1992; Taylor 2000).
Originally described from Cuba (Poey 1880), the
species has since been slowly documented as far
north as central Florida, USA, north through the
Yucatan Peninsula and Bay of Campeche in Mexico,
along almost the entire Central American and northern
South American coastline, and likely south to the
mouth of the Amazon River. However, records east
and south of Venezuela are sparse (Huber 1992).

The species designation on the South American continent remains confused. The International Commission on Zoological Nomenclature (ICZN, Case no.
2722, 1992) gave precedence to Rivulus marmoratus
and relegated Rivulus ocellatus to the formers synonymy. However, recent molecular evidence supports
separation of the two species (Tatarenkov et al. 2009,
2010), and suggests that the ocellatus lineage is found
as far north as Panama and southern Cuba. Biogeography theory might suggest that K. ocellatus is found
from southern Brazil north to the mouth of the
Amazon River, while K. marmoratus is found further
north. A third taxon, K. marmoratus bonairensis, the
subspecies from the Netherlands Antilles is now generally disregarded, and reclassification of the Brazilian
species continues (Costa 2011). However, more extensive collections subjected to morphological/meristic
and molecular analyses are required over the entire
South American coastline before the nomenclatural

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D. Scott Taylor1

Ecology of mangrove rivulus

Habitats
As the common name mangrove rivulus implies,
K. marmoratus is affiliated closely with and spends its
entire life cycle within mangroves, and the distribution of the fish tracks closely with that of the red
mangrove, Rhizophora mangle. Only one other fish is
a true mangrove-affiliate, the poeciliid Gambusia
rhizophorae (Davis et al. 1995). In fact, stable isotope
data for K. marmoratus from Everglades, Florida, and
Twin Cayes, Belize indicated a strong mangrove
signal (C. C. McIvor, unpublished data).
Part of the presumed rarity of K. marmoratus is due
to looking in all the wrong places. Conventionally

minded ichthyologists are at a disadvantage, and the

fish must be sought within a suite of micro-habitats
within the mangroves. The list is rather incongruous:
intermittently dry shallow, stagnant pools; crab burrows (specifically, those of Cardisoma guanhumi,
great land crab, and Ucides cordatus, mangrove land
crab); temporally flooded swales; ditches (including
anti-mosquito ditches); inside/under logs and mangrove leaf litter; solution holes; empty beer cans and
coconuts; and even several meters inside anchialine
cave systems (Taylor 2000; Taylor et al. 2003, 2008).
A common denominator among these micro-habitats
includes their being either fossorial, intermittently dry,
or having adverse water quality conditions that
preclude the establishment of other species of fish.
Perhaps Harrington and Rivas (1958) have aptly
summarized the conditions favored by K. marmoratus
in their description of some collections from antimosquito ditches in east central Florida: water
. . . turbid to opacity, and the ditch bottoms were
mostly treacherous, malodorous, marly muck . . . .
Such a description might not inspire most ichthyologists, and this passage alone may account for the paucity of K. marmoratus in collections.
The specific identification of crab burrows
(C. guanhumi, U. cordatus) as a focus of K. marmoratus habitation has expanded the extent of collections, both geographically and numerically, thereby
revising the impression of the fishs rarity (Davis
et al. 1990; Taylor 2000). The fossorial nature of
K. marmoratus figures prominently in its natural history, and we may be underestimating the use of
smaller crab burrows (e.g., Uca spp.), which are as
yet impossible to sample. These may serve as refuges
during low water. Kryptolebias marmoratus have frequently been observed entering Uca spp. burrows
when dropped during field collection or during
very low water (D. S. Taylor, unpublished data). In
addition, McIvor and Silverman (2010) and Richards
et al. (2011) collected large numbers of K. marmoratus in the intertidal mangroves during tidal flooding
at both Shark River, Everglades, FL and Tampa Bay,
FL, where the only refuges during low water appear
to be smaller crab burrows (Uca spp. and mud crabs
[Eurytium limosum]). Larger burrowing crabs
(C. guanhumi and U. cordatus) are not found in
any significant numbers from Florida Bay up the
western coast of Florida (personal observation).
Similarly, at the northern extent of the fishs range
on the eastern coast of Florida (Volusia County), the
only fossorial habitats available at low water are

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issues can be resolved. Recent collections just south of

the Amazon River do confirm the presence of a Kryptolebias sp. (M. Barletta, personal communication)
North of the confusing South American picture,
K. marmoratus is presumably found throughout all
of the Antilles and Bahamas, including the island of
Barbados, far to windward. This remarkable and
widespread distribution is clearly a tribute to waif
dispersal and the evolutionary advantage of the ability to find a population from a single progenitor.
The ultimate proof of the latter supposition would
be documentation of the presence of the fish on the
island of Bermuda, the most distant extension of the
tropical Atlantic and the neotropical mangrove ecosystem. However, the fish has yet to be recorded
there, and in 2007 a brief survey within the very
limited mangrove habitat did not produce this fish
(D. S. Taylor, unpublished data).
In spite of its extensive distribution, K. marmoratus has been frequently described as rare: It is
undeniable that (Rivulus) marmoratus is rare and
little known in the wild . . . , by Harrington and
Kallman (1968). Serious students of K. marmoratus
in the field now recognize that this is overstated, but
even so the state of Florida has listed K. marmoratus
as a Species of Special Concern. Kryptolebias marmoratus is also a Federal Candidate Species for
listing by the NMFS (National Marine Fisheries
Service) (Fed. Reg. 62:(134) 7/14/97), but there is
no current Federal listing, nor does any other
nation list the species. The current listing for
Florida is being reevaluated, but it has been pointed
out that in at least some portions of the State, the
species has been adversely impacted by development
and by hydrologic alteration of tidal wetlands
(Taylor 1999).

725

726

burrows of Uca and Eurytium and rotten logs.

However, K. marmoratus at their northern range
on this coast has presented other puzzles, including
an apparent outlier population that is disjunct from
those to the south by 105 km (Taylor 2000). In addition, the most recent collection from this region (2009)
was obtained from a benthic sample by scraping the
fouling growth on the pontoons of a floating restaurant (C. Macfie, personal communication).

Environmental physical parameters

Kryptolebias marmoratus is perhaps more tolerant of
temperature extremes than are some other tropical
species and it has been collected over a wide thermal
range (7388C) (Taylor et al. 1995); there is evidence
that the fish can survive 58C when emersed (out of
the water) (Taylor 1999). Extreme cold has resulted
in documented cold mortality at the northern
extreme of the fishs geographic range (central
Florida), a hazard common to all tropical fish species
found at the limits of their ranges (Taylor 1993).
Falling temperature seems to induce emersion in a
laboratory setting (Huehner et al. 1985), but the
adaptive value of this is unclear, and no comparable
study looking at the effects of increasing temperature
has been carried out. Clearly, fossorial niches (e.g.,
crab burrows) offer a thermal refuge during cold
events. During a cold event in Florida, water temperature inside Cardisoma burrows remained at
168C, while nearby shallow pools were 108C, a temperature fatal to many tropical fishes (Taylor, 1992;
Gilmore et al. 1978). However, if these types of fossorial refuges are not available, and, in fact emersed
fish are more resistant to low temperature, the laboratory observations of increase in emersion with
falling temperature (Huehner et al. 1985) may indicate that such emersion has survival value.
Low temperature is probably the primary factor limiting northern distribution at the extremes of range in
Florida, but ranges do not appear to be equivalent on
both coasts. A search for K. marmoratus on the western
coast of Florida (offshore islands of the Cedar Key area)
was completed at the equivalent latitude (298 050 ) of
the known northern limit on the eastern coast. No
specimens were found at Cedar Key, although the
habitat appeared ideal, and this may reflect lower
temperature regimes on the western coast of Florida
(D. S. Taylor, C. C. McIvor, and W. P. Davis, unpublished data).

Salinity
Kryptolebias marmoratus is euryhaline and has been
collected in the wild at salinities of 070 ppt
(Kristensen 1970; Taylor et al. 1995), and in the laboratory juveniles can tolerate 7080 ppt (Taylor
2000). While it is noted that K. marmoratus can be
reared and will reproduce in fresh water (Huber
1992; Lin and Dunson 1995), collections at very
low salinities in the wild probably reflect temporary
conditions following heavy rainfall (unpublished
data). In natural habitats where there is a gradient
from pure fresh water to saline mangroves (e.g.,
Everglades, Florida), K. marmoratus were not found
except in areas with salinity 410 ppt (D. S. Taylor
and W. P. Davis, unpublished data). Taylor (1999)
reported that attempts to introduce K. marmoratus
into isolated freshwater pools in the field were unsuccessful, except in one instance where the site intermittently dried and no species of fish were
present. The abundance of freshwater invertebrate
predators may also prevent recruitment of juvenile
K. marmoratus (D. S. Taylor, unpublished data).
In contrast, extreme salinities are a common feature of mangroves during drought or periods of
reduced tidal inundation. Adaptation to hypersaline
conditions in teleosts is partially contingent upon
activity of chloride cells. King et al. (1989) found
that the chloride cells in the opercular epithelium
and opercular skin increased in size (up to
39100% larger) in K. marmoratus raised at 100
and 200% seawater versus fish raised at 1% seawater.
The overall number of chloride cells, however, did
not increase at elevated salinities. This study also
reported that in laboratory transfer studies,
K. marmoratus could adapt to 114 ppt seawater.
Hydrogen sulfide
Hydrogen sulfide (H2S) is widespread in marine
environments and it is well-known that it is toxic
to fish (Bagarinao and Vetter 1989); it is common
in surface and porewaters of mangrove systems.
Anyone venturing into the mangroves is familiar
with the characteristic rotten egg smell. In addition to direct toxicity, H2S quickly scavenges any
available dissolved oxygen, presenting a double challenge to aquatic life. Hydrogen sulfide is likely a key
driver of emersion behavior (see below) in K. marmoratus, but there are few field studies on the concentrations of H2S in K. marmoratus microhabitats.
Abel et al. (1987) measured H2S at 0.40.7 ppm in a

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Temperature

D. S. Taylor

727

Ecology of mangrove rivulus

Ammonia
Frick and Wright (2002a) investigated ambient ammonia levels in Belizean U. cordatus burrows known
to contain K. marmoratus. They found that ammonia
averaged about 1 mmol/L, a level greater than that
typically found in most other aquatic habitats, fresh
or saline. Since they determined that K. marmoratus
can tolerate levels 410 mmol/L, the observed levels
would not appear to significantly stress the fish
but, as with H2S, lack of tidal/rainfall flushing

might allow levels to elevate further. The pH of the

water in burrows was also measured in their study,
and found to be lower than in the adjacent open
ocean (pH 7 versus pH 8). However, these lower
pH values may mitigate potential toxic consequences
of ammonia. The lower pH observed in burrows may
be the result of H2S production or result from the
metabolic activities of resident crab(s) and/or fish
(Frick and Wright 2002a). Further complicating the
chemical soup found within crab burrows is the
reduced tolerance of fish to ammonia at lower salinities (Frick and Wright 2002a), and, as noted, salinities can drop drastically following heavy rainfall.
An extensive array of physiological adaptations is
clearly required for K. marmoratus to thrive in the
mangroves.
Dissolved oxygen
Other than H2S, another ubiquitous feature in mangroves is the common occurrence of low dissolved
oxygen (DO). Kryptolebias marmoratus, as noted,
have frequently been collected under conditions of
very poor water quality, and have been documented
to survive hypoxic conditions (51.0 ppm) in the field
(Dunson and Dunson 1999). While, conditions this
extreme may be uncommon and usually occur at
night, a series of 149 DO readings in flooded
K. marmoratus habitat in Belize over several days on
two different years found a mean DO of 2.39 ppm
(D. S. Taylor, C. C. McIvor, E. Reyier, and
W. P. Davis, unpublished data). However, extremes
of low DO can occur in isolated mangrove pools in
Belize, where a 1-day survey of several pools containing K. marmoratus at very low-water found DO ranging from 0.16 to 0.98 (D. S. Taylor, P. Molloy, and
M. Fish, unpublished data). Finally, DO was measured
across a suite of six different mangrove habitats (as
described by Feller et al. [2002]): fringe, transition,
dwarf red, creek, pond, and sinkhole. These data indicate that the sinkhole habitats (where K. marmoratus
are regularly found) had the lowest DO, followed by
the transition zone (the higher elevations where
K. marmoratus would typically be found in burrows
and pools). This parameter partially explains the
paucity of other fish species in the internal mangroves.
Finally, it has only been recently determined that
hypoxia (0.2 mg/L) is known to induce emersion in
the laboratory (Regan et al. 2011).
Survival in environments with low DO may require
fish to be physiologically adapted for surface aerial
respiration (SAR), in which the oxygen-enriched

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one-time survey of inundated mangrove pools that

contained K. marmoratus in southwestern Florida.
These data may actually represent more benign
conditions, as Carlson et al. (1983) found maximum
H2S levels of 51.1 ppm in pore water on Floridian
mangrove islands. Rey et al. (1992) measured H2S in
pore water as high as 1.64 ppm in mangrove/saltmarsh wetlands in east central Florida. In a very
limited study of H2S within U. cordatus burrows in
Belize, concentrations varied from 0.59 to 10.59 ppm.
Concentrations did not vary significantly between
surface water in the burrow and water at 8 cm
depth, but when incoming tides flooded the burrows,
H2S levels dropped quickly. In general, burrows
further from the oceanic open water exhibited
higher levels of H2S (D. S. Taylor, unpublished
data). While the levels of H2S observed in Belize
are likely not sufficient to be fatal to K. marmoratus
(tolerant estuarine species had a 96 h LC50 of 17.8
23.8 ppm [Bagarinao and Vetter 1989]), avoiding
elevated levels may be a constant challenge for
K. marmoratus.
During low-water periods, K. marmoratus within
crab burrows and stagnant pools frequently develop
a white coating on the skin and fins (Taylor 2000;
Taylor et al. 2004). If specimens displaying these features are captured and placed in fresh seawater, the
coating disappears and attempts to scrape the material off the fish and preserve it have been unsuccessful (D. S. Taylor, unpublished data). It was
previously suggested (Davis et al. 1990) that this feature was mucus produced in response to adverse
water quality, but it seems more likely that it is the
actual growth of a sulfur-oxidizing bacterium
(Beggiatoa sp.). This bacterium is frequently seen
coating the surfaces of water or substrate in high
sulfide mangrove settings and has also been seen
growing on the epidermis of poeciliid fishes living
in H2S enriched artesian flows from wells in
Florida (D. S. Taylor, personal observation).

728

Diet
There are limited studies of the diet of K. marmoratus in the wild, but this fish is clearly a predator,
with various terrestrial and aquatic invertebrates
forming the bulk of the diet. Harrington and Rivas
(1958) provided the first insights into its diet,
although from the guts of only two specimens
from mosquito ditches, and found mosquito larvae,
a snail, a crab, and an adult stylops (an insect parasite). Kristensen (1970) supplemented this information, reporting that K. marmoratus from the
Netherlands Antilles consumed gastropods, various
crustaceans, dipterans, formicids, and juvenile
fishes. Huehner et al. (1985) collected emersed fish
in the Florida Keys and analyzed the guts of 21 specimens; they found mosquito larvae, fish parts, polychaetes, copepods, and miscellaneous insects. Both
Kristensen (1970) and Taylor (1988) indicated that
K. marmoratus is cannibalistic. The most comprehensive study of diet to date, 111 specimens collected
from the burrows of C. guanhumi in east-central
Florida, found that 60% of guts were empty
(Taylor 1992). This relatively low frequency of

feeding may indicate a paucity of food resources in

the marginal, intermittently dry microhabitats where
the fish is found. Periods of flooding by rainfall or
tidal inundation could provide enhanced feeding opportunities and also allow K. marmoratus priority
feeding, as other fish species would be moving
from sources of permanent water, for example estuarine water itself or permanent ponds/creeks within
the mangroves (Taylor 2000). Of the guts containing
food items, 41% contained items of terrestrial origin
(dominated by unidentified insect parts) and 92%
contained items of aquatic origin (mostly polychaete
parts and gastropods). It appears likely that the latter
dietary items originated within the crab burrows
themselves, as during the study period the 111 specimens were likely confined to the burrows, due to
lack of tidal/rainfall flooding (Taylor 1992).
However, since the infauna of crab burrows is largely
unstudied, the exact origin of these food items
cannot be determined. In addition, although it is
known that K. marmoratus will leave the water to
capture food and return to the water to consume it
(Huehner et al. 1985; Taylor 1990), the extent of this
behavior is unknown. It is clear that to some
degree crab burrows serve as pit-traps for insects,
and some of the predation on insects by K. marmoratus has been observed at night (Taylor 1992).
During flooding events it is likely that fish range
some distance from their burrows for feeding, and
several fish have been observed attacking a moth that
had fallen onto the waters surface (D. S. Taylor,
personal observation).
The saltmarsh mosquitoes, Aedes taeniorhynchus
and Ae. sollicitans, are known to oviposit in some
of the microhabitats occupied by K. marmoratus
(e.g., intermittently dry pools and mosquito ditches,
as larvae are frequently observed here (D. S. Taylor,
personal observation; Ritchie and Johnson 1986). It
is therefore likely that mosquito larvae are a frequent
dietary item. Both laboratory and field studies have
confirmed heavy predation by K. marmoratus on
saltmarsh mosquito larvae (Taylor et al. 1992). In
the laboratory, K. marmoratus of 40 mm standard
length (SL) consumed up to 80 larvae in 24 h, and
even juvenile fish (1-day old) ate a maximum of 21
newly-hatched larvae (Taylor et al. 1992). These feeding rates meet or exceed those of well-known mosquito larvivores (Gambusia spp.) (S. A. Ritchie and
E. Johnson, unpublished data). Yet, natural populations of K. marmoratus never seem to reach the densities seen in larvivorous poeciliids (Gambusia), so

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surface layer of the water is utilized in respiration.

Kryptolebias marmoratus, with its flattened head, upturned mouth and small size (Lewis 1970) exhibits the
physical characteristics allowing SAR. In addition to
these features, an enhanced capillary network is
found in the dorsum of the epidermis, within 1 mm
of the surface. This feature is not found on the ventral
surfaces (Grizzle and Thyigarajah 1987). These
capillaries are most dense on the nape, decreasing posteriorly until becoming absent past the dorsal fin. All
ages/sizes of fish illustrated this same pattern (Grizzle
and Thyigarajah 1987). Partial emersion, whereby K.
marmoratus place themselves at the waters edge/surface, typically lodged against/under debris, is frequently seen in the field, as well as short-term bouts
of SAR while actively swimming and skimming the
surface (personal observation). The anatomical features described, therefore, are clearly adapted for
these behaviors. The importance for this species of contact with the air/water interface is emphasized by repeated observations of fish drowning if retained in
traps beneath the water, often only for very short
periods. Such fish display classic symptoms of anoxia,
with flared, pale gills, but the influence of H2S in these
mortalities is unknown (Davis et al. 1990; D. S. Taylor,
personal observation).

D. S. Taylor

Ecology of mangrove rivulus

their direct contribution to mosquito control is

perhaps limited.

Emersion

possibly provide protection against abrasion and desiccation when emersed (Grizzle and Thyagarajah
1987). Additionally, mucus enhances adhesion to
vegetation and other surfaces during terrestrial
movements. Finally, epidermal blood vessels in the
fins very likely aid in aerial respiration (Grizzle and
Thyagarajah 1987). Remarkably, emersion results in
no overall change in metabolic rate compared to fish
in water (Ong et al. 2007), although Abel et al.
(1987) previously reported that oxygen consumption
both in adult and juvenile K. marmoratus was significantly less when emersed.
Within the gills of emersed fish, there is a decrease
in the surface area of the gill lamellae and an increase
in the cell mass between the lamellae (Ong et al.
2007). This remodeling of the gills, which occurs
after 1 week out of water, is reversible and fish returned to water restore normal morphology of the
gills after another week. The growth in the cell mass
between the lamellae is thought to keep the lamellae
from collapsing, which could inhibit respiration
upon returning to water, and possibly also enhances
branchial aerial respiration, as well as resist overall
desiccation of the gills.
Having conveniently solved the problems of desiccation and the respiratory complications of emersion, one further remarkable adaptation remains:
mode of ammonia excretion. Litwiller et al. (2006)
and Frick and Wright (2002b) determined that 42%
of ammonia excreted during emersion was via volatilization, and that the cutaneous surface is the site of
this process; there the highly vascularized surface of
the skin again comes into play.
Huehner et al. (1985) were among the first to look
at the details of emersion behavior in the field and
laboratory. They were also the first to note an apparent knowledge of terrestrial landscapes by the fish.
When recently emersed fish in the field were exposed
by turning over logs, they would flip up to 0.5 m
away with some accuracy, to disappear down crab
burrows or burrow into leaf litter. Taylor (1990)
also demonstrated this in a laboratory microcosm
containing crab burrows; there fish were free to
move overland between two burrows separated by
8 cm of mud. Fish appeared highly motivated to
switch burrows, one fish doing so six times in 24 h.
When a plexiglass barrier was erected in the mud
between the two burrows, this movement ceased,
but time-lapse videography showed repeated attempts to cross the barrier. Further, when a small
hole was subsequently drilled in the barrier at the

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Emersion is well-known among K. marmoratus and

some of its congeners (approximately 100 species;
Huber 1992) and is a comprehensive term that includes both active movement out of the water (wiggling/flipping across a damp substrate) or the more
torpid state achieved during more long-term emersion (Taylor 1990). Kristensen (1970) was the first to
describe emersion in K. marmoratus, where he documented specimens from the Netherlands Antilles
emersed within damp algal mats and also moving
overland as follows: When their habitat dries up
they are able to find their way back to the water
by jumping, crawling, and wiggling through wet pebbles and mud, covering distances of dozens of
meters.
As noted, one physical driver of emersion is excessive H2S. Although data are limited, Abel et al.
(1987) determined that in the laboratory 50% of
K. marmoratus left the water at an H2S concentration
of 0.12 ppm, a level extraordinarily low compared to
known field levels (D. S. Taylor, unpublished data).
The duration of emergence in the laboratory was
correlated with the concentration of H2S; and at
lower concentrations, fish tended to ventilate at the
surface more but did not emerse. No effect of hypoxia on emergence was noted (Abel et al. 1987;
Taylor 1990), although neither of these studies
looked at the low levels (0.2 mg/L) now known to
induce emersion (Regan et al. 2011).
Harrington and Rivas (1958) reported that
K. marmoratus was the last species to be affected
by rotenone, a toxicant targeting the gills, compared
to 28 other fish species taken in association with
it. This apparent resistance to rotenone is more likely
the result of emersion as a means of avoiding it.
Intra-specific aggression can also lead to emersion
in both the field and laboratory (Taylor 1988,
1990). The role of other parameters of water quality
(ammonia, salinity, and temperature) has not been
extensively examined as yet.
A number of other morphological/physiological
adaptations enhance the ability of K. marmoratus
to emerse. In addition to the cutaneous features described above, the ventral surface of the fishs head
region has a thicker epidermis that contains goblet
cells producing mucus. Both of these features

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will enter artificial logs in aquaria as water levels

decline, but often waited until the log was out of the
water, necessitating traveling across a dry substrate
(D. Bechler, personal communication). However, in
the wild, fish may traverse a considerable distance
once inside the logs, with some individuals being
found 20 cm from obvious entrance holes. The densities observed inside these logs are remarkable: 100
individuals inside a section 1.5 m long and 9 cm in
diameter (Taylor et al. 2004). Individuals are closely
packed together, exhibiting enhanced mucus production (D. S. Taylor, unpublished data), but become
active immediately upon being exposed, either flipping out of the galleries or attempting to slither further into the interior (Taylor et al. 2008).
Cessation of intra-specific aggression when fish are
emersed has been noted in this species, which can be
quite aggressive in water (Taylor 1990; Huehner et al.
1985). There may also be as-yet undocumented physiological benefits to emersion in groups with close
physical contact, for example reduced metabolic rates
(Taylor et al. 2008). Laboratory rearing in community tanks (many individuals of a common lineage
in the same tank) has also revealed differences in
emersion behavior between clones, with some
clones emersing more frequently and others emersing
in compact groups of multiple individuals. This behavior is being further investigated (D. Bechler, personal communication) However, the clear survival
value of emersion is very apparent in the field
when other fish species (e.g., poeciliids) have been
found dead in drying pools and crab burrows known
to contain K. marmoratus, with K. marmoratus
emersed above the floating corpses (Taylor 1990;
Abel et al. 1987).

Predation
Few instances have been documented of predation
on K. marmoratus. There are two records of predation by wading birds (Wood Stork, Mycteria americana and Tricolored Heron, Hydranassa tricolor) as
determined from regurgitates (Taylor 1999). But
overall, wading birds do not seem to frequent the
small ponds and heavy mangrove cover where
K. marmoratus is found (D. S. Taylor, personal
observation), with the exception of smaller species
like the green heron (Butorides virescens). Given the
extremely secretive and fossorial nature of the fish, it
is hard to envision intense avian predation (Taylor
1999). Kristensen (1970) proposed that predation by

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surface of the mud, the fish found the opening and

resumed movement. Some of the activity occurred at
night (Taylor 1990).
In their limited laboratory study of the effects
of temperature on emersion, Huenher et al. (1985)
found that fish preferred being in water at
258C, moving to land as temperatures dropped to
19208C, but even then fish would temporarily
return to water. The authors speculated that emersion during dry-down prevents the concentration of
K. marmoratus at the edge of the mangroves, where
predation is greater. Re-flooding would then result in
immediate resumption of aquatic activity, within the
original occupied territory. Fish that emersed for
412 h were less responsive to mechanical stimulation,
requiring prodding before movement. In many cases
in the wild, emersion is clearly the result of drying of
the habitat, often over an extensive period. Taylor
(1990) found that K. marmoratus can survive at
least 66 days out of the water in the laboratory.
The study animals were emaciated (31.4% weight
loss), but upon reflooding they immediately resumed
feeding and normal activity.
Taylor et al. (2004) described two patterns of
emersion in Belizean K. marmoratus: (1) under
debris (including sheets of plastic and lumber), leaf
litter, inside logs, and (2) onto the sides or mouths
of crab burrows. The former cases are probably
long-term and occur when temporary pools have
dried or water quality within crab burrows has degraded. Emersion within a crab burrow was of
shorter term, and fish often reentered the water several times within an hour. The incidence of this
short-term emersion in burrows seemed to increase
at night, when it is likely that water quality declines
(D. S. Taylor, personal observation).
Multiple fish are known to emerse inside rotting
mangrove logs on the forest floor, resulting in very
high concentrations of animals (Taylor et al. 2004,
2008). This phenomenon (termed log packing)
occurs inside logs that have been galleried by beetle
larvae and termites, which subsequently fall into
shallow pools in the mangroves. The galleries are
1020 mm in diameter in many cases riddling the
logs, and are full of a sawdust-like frass, the byproduct of insect activity. These logs remain spongy and
water-saturated for a considerable period of time
after dry-down (D. S. Taylor, unpublished data).
How and when fish enter the logs is unknown, but
it likely occurs as the pools near final dry-down.
Some preliminary laboratory data show that fish

D. S. Taylor

731

Ecology of mangrove rivulus

Parasitism
Kryptolebias marmoratus has never been noted to
display any of the classic teleost skin diseases
(Ich or other white-spot diseases) in either laboratory or field populations (Taylor 1999). Rarely, in
Floridian populations an unidentified fungal pathogen was seen on the body and fins (Taylor 1999),
and a digenean trematode was seen in a Brazilian
museum specimen (D. S. Taylor, unpublished data;
E. H. Williams, personal communication). Whether
the species is innately more resistant to external parasites than most other species, or the exposure to
parasites is not as frequent in the marginal habitats
that the fish occupies, remains to be seen. However,

a recent study (Ellison et al. 2011) demonstrated that

among Belizean K. marmoratus with varying rates of
genetic heterozygosity, more heterozygous fish had
fewer internal parasites than did homozygous fish.
However, all fish were infected with one of three
different parasites: bacterial cysts on the gills,
Trichodina (a protozoan), or acanthocephalans.

Competition
As noted, other species of fish are not commonly sympatric with K. marmoratus, presumably
due to the demanding physical regimes of their
preferred microhabitats. Only a few other species
(e.g., Gambusia spp., Poecilia spp., Fundulus spp.,
Cyprinodon spp., Adenia xenica, and D. maculatus)
have been collected in any significant number in
the intermittently flooded swales/potholes/ditches
where K. marmoratus may be found. One exception
to this was McIvor and Silverman (2010), where
greater diversity was found in riverine forests along
Shark River, Everglades. However, most, if not all of
these fishes, leave with receding tides or do not survive periodic dry-down (Abel et al. 1987; Davis et al.
1990; Taylor 1990; D. S. Taylor, unpublished data).
Conversely, K. marmoratus is rarely taken in mangrove habitats with permanent water. No studies,
either field or laboratory, of competition between
K. marmoratus and these sympatric species have
been conducted, and the reason(s) that K. marmoratus is not more often found in permanent waters is
unknown (Taylor 1999). Dunson and Dunson (1999)
found a similar situation (relatively few sympatric
species present) on the western coast of Florida,
south of Tampa Bay. In their field collections of K.
marmoratus, they noted that at the higher elevations
K. marmoratus occupies, abiotic conditions are too
extreme to allow other competitively superior small
fishes (e.g., Gambusia) to survive. McIvor and
Silverman (2010) studied K. marmoratus in the
Shark River, Everglades National Park, FL and
found 21 other species of fish species associated
with it, but only six species (including K. marmoratus) made up 90% of their bottomless lift net catch
and two species (K. marmoratus and a palaemonid
shrimp) comprised 75% of the catch.
A congener, Rivulus tenuis, is commonly found
sympatric with K. marmoratus in crab burrows/potholes on mainland Belize. Rivulus tenuis is a dioecious, freshwater form (Huber 1992), but was found
in salinities up to 10 ppt (Taylor et al. 2004) in 2000

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other fish is probably minimal, as K. marmoratus is

so secretive and cryptic. Estuarine piscine and crustacean predators (e.g., snapper, barracuda, and blue
crab) do move into K. marmoratus habitat during
periods of heavy tidal flooding (personal observation) and there may be incidental predation on
K. marmoratus then. McIvor and Silverman (2010)
documented several potential predators in association with K. marmoratus in Everglades, FL mangrove
lift-net collections, including a few goby species,
Cichlasoma uropthalmus, Belenesox belizanus (these
two species were also documented in Belize mangroves [Taylor et al. 2007]), and Strongylura notata.
Three species of eleotrids, Guavina guavina,
Dormitator maculatus, and Eleotris pisonis have been
documented inhabiting crab burrows (Taylor 2001),
and all three are known to prey upon other fishes
(Teixeira 1994; Taylor 2001). However, the only
direct evidence of predation on K. marmoratus is
in one instance when E. pisonis was found to prey
on them in pits of brackish water (Kristensen 1970).
However, where G. guavina was present in large/
deeper U. cordatus burrows in Honduras, which normally might have contained numerous K. marmoratus, none was found. These same Guavina, however,
freely preyed upon Gambusia sp. presented on a
baited hook (Taylor 2001).
A more significant predator may be the mangrove
water snake, Nerodia fasciata compressicauda,
mis-identified as the Atlantic saltmarsh snake (N. f.
taeniata) by Taylor (1990), which is seen in crab
burrows and mangroves in Florida and Belize.
Predation on K. marmoratus by this species has
been confirmed in Belize (D. S. Taylor, unpublished
data).

732

Population density/movement
In some locales, K. marmoratus is no longer considered rare, with a single crab burrow having produced 26 individuals (Taylor 1990) and catches from
other burrows and potholes sometimes in excess
of ten individuals not uncommon (Taylor 1992;
D. S. Taylor, unpublished data). In a preliminary
survey of K. marmoratus on a Belizean offshore cay
(Twin Cayes) transition mangroves (an area of predominately black mangroves [Avicennia germinans])
inland from the fringing red mangroves), Taylor
et al. (2007) erected small fiberglass screen enclosures
during low tide (the sites then being dry and all
K. marmoratus presumably undergound). The enclosures were then removaltrapped to depletion with
cup traps (small plastic cups fitted with a funnel for
sampling within crab burrows or very shallow water
[Taylor 1990]) at each tidal flooding. Four areas were
enclosed, varying in size from 0.75 to 2.2 m2.
Although complete integrity of the sites could not
be assured, as there may have been underground
connections via crab burrows, the density of K. marmoratus varied from 7 to 26 fish/m2, remarkable
numbers when considering that the transition is basically intertidal. At another Belizean cay (Calabash
Cay), four other enclosures (0.802.41 m2) produced
from 2.5 to 13.4 fish/m2 (D. S. Taylor, unpublished
data).
McIvor and Silverman (2010) utilized a modified
6 m2 bottomless lift-net in riverine mangroves in the
Everglades. In their extensive study, nets were
deployed 189 times at three locations over 7 years,
and 21 species of fish were taken, numerically dominated by K. marmoratus. Overall, density of K. marmoratus was 0.39 fish/m2. Kryptolebias marmoratus
were most abundant at the higher elevation site
with the least tidal flooding, and with lower density

of fishes in general and least overall diversity of fish.

Conversely, K. marmoratus were least abundant
where tidal flooding was greatest, that is, at lower
elevations (C. C. McIvor, personal communication).
Further north in Florida, in the Tampa Bay area,
Richards et al. (2011), noting a lack of data linking
microhabitat variables to abundance of K. marmoratus, utilized trench traps sunk in the forest floor and
found that K. marmoratus was the numerically dominant species of fish in mosquito-ditched intertidal
mangroves. Kryptolebias marmoratus were more
abundant further away from permanent water-filled
mosquito ditches. Higher catches were associated
with greater amounts of leaf litter. No association
was found between number of fish and abundance
of crab burrows (fiddler crabs and mud crabs: Uca
sp. and E. limosum). Since no fish were observed
among the leaf litter at low tide, it is assumed that
they were retreating down crab burrows at that time.
The density of burrows was high (24256/m2), and
it may be that burrow density is not limiting, so
no correlation between density of burrows and
abundance of fish was seen (Richards et al. 2011;
C. C. McIvor, personal communication)
The movement of individual K. marmoratus in the
field remains largely unstudied. In Belize, 14 marked
(unique fin-clip) fish were released in their burrows
of origin. Repeated cup trapping (in burrows and on
the surface of the sediment) over several days within
an area of several meters adjacent to capture sites
resulted in only two marked recaptures, although a
total of 81 fish was taken in the recapture effort. One
marked fish had moved a maximum of 7 m from
burrow of origin in 5 days, while the other had
moved 1.5 m. However, the sizes of the fish captured
from the same burrows over time were noted, and
there was little repeatability in size, indicating a
high turnover of occupants, while the low recapture
rate again attests to high population density
(D. S. Taylor, P. Molloy, and M. A. Fish, unpublished data).

Oviposition/habitat of juveniles
In a laboratory setting, observations in the crab
burrow microcosm described by Taylor (1990)
suggested that wild fish strand their embryos, a
trait rather common among the genera Rivulus and
Kryptolebias (Huber 1992), and in fact, much of this
behavior may occur at night (Taylor 1990). However,
repeated searches for embryos in the field largely

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at Dangriga, Belize. The potential competitive interactions of these two species merits further attention.
Up to four R. tenuis were found in a single crab
burrow along with one K. marmoratus. At the same
site, up to ten K. marmoratus were found in a single
burrow along with one R. tenuis. Overall, 46 K. marmoratus were collected along with 13 R. tenuis
(Taylor et al. 2004). However, near this same site
in 2006, salinities were slightly higher (1416 ppt)
and 60 K. marmoratus were taken with no evidence
of R. tenuis (D. S. Taylor, P. Molloy, and M. A. Fish,
unpublished data).

D. S. Taylor

Ecology of mangrove rivulus

amount of heterozygosity exists, suggesting possible

hermaphrodite/hermaphrodite crossings (Mackiewicz
et al. 2006c). Hermaphrodite/male outcrossing has
been documented in the laboratory (Harrington
and Kallman 1968; Mackiewicz et al. 2006a) and,
given the general difficulties of observing this cryptic
animal in its complex natural environment, it is not
surprising that there has been no visual confirmation
of outcrossing (or oviposition) in the field. Given that
oviposition may take place out of the water, there are
obvious complications to outcrossing. Nevertheless,
observations in aquaria, in which wild Floridian hermaphrodites were presented with brightly colored,
wild Belize male fish, suggest that the innate behaviors
for outcrossing are there. When the male fish
approached the hermaphrodites near spawning
mops at the top of the aquarium, the two sexes displayed many of the classic killifish courtship/spawning
behaviors: recurved bodies coupling closely and vibrating (D. S. Taylor, unpublished data). Such behavior is
rather incongruous, given that male fish are unknown
from these Floridian populations and the general intraspecific highly aggressive tendencies normally seen
between individuals in aquaria.
The embryos are not the only early life-history
stage that is little-known, as few juveniles (510 mm
SL) have been found in the wild. Harrington and
Rivas (1958), using rotenone to collect in mosquito
ditches in east-central Florida, have the most documented success with 22 very small juveniles
(7.511.1 mm SL) having been taken. These collections occurred in August, implying that oviposition
and hatching occurs earlier in the summer. Taylor
(1999) reported about a dozen small fish (715 mm
SL) taken from crab burrows in autumn and winter
in east-central Florida. Given the propensity for cannibalism in this species, the fact that no fish smaller
than 7 mm SL has ever been taken from a crab
burrow suggests that juveniles may largely be occupying as-yet unidentified micro-habitats (Taylor
1990). Of the 161 total specimens taken by
Richards et al. (2011) from Tampa Bay, size ranged
 16.8 mm), including one
from 7 to 35 mm SL (
cohort of 25 individuals (711 mm SL) taken at
the end of June, again, likely a result of oviposition
in early summer. Overall, specimens from Tampa
Bay were notably smaller than those from two
other Floridian populations examined: Shark River,
Everglades, and east-coast Florida (Richards et al.
2011; Taylor 1992). This reduced size was attributed
to the lower temperatures encountered at more

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have proved fruitless, with only a few embryos found

on the sides of crab burrows and several secreted
within leaf litter at the exposed margins of stagnant
pools (Taylor 1999; D. S. Taylor, unpublished data).
Kryptolebias marmoratus embryos will develop
fully without standing water, provided they are
kept damp (Taylor 1990). Embryos apparently
enter a diapause when fully developed, holding
at full development and then finally hatching when
flooded. This has been observed both in the laboratory (personal observation) and in the field, where
newly-hatched K. marmoratus appeared immediately
after reflooding of dried mangrove pools where
adult fish were known to be present (Ritchie and
Davis 1986).
Very large (4055 mm SL) wild gravid hermaphrodites in both Belize and Florida have been known
to release large numbers of viable embryos (approximately 50 or more) in mass spawnings within
collection containers after capture (Taylor 2000;
D. S. Taylor, unpublished data). While this may be
a response to the stress of capture, the prospect for
deposition of large numbers of embryos in a single
oviposition event in the wild seems likely. However,
where oviposition occurs, remains one of the more
enduring mysteries of the fishs natural history; given
the apparent density of many populations, there
must be many embryos present.
In the tropics, it is safe to assume that reproduction occurs year-round, except for prolonged
droughts and/or low tides. We have seen reproduction in the laboratory immediately following capture
at all times of the year in Belize (W. P. Davis and
D. S. Taylor, unpublished data). In the sub-tropics
(e.g., Florida), there are some data on K. marmoratus
gonads that support a hiatus in reproduction during
cooler weather. Taylor (1993) examined 111 gonads
from phenotypic hermaphrodites from east-central
Florida. Most fish (n 108) contained developing
or mature eggs within the ovotestes; but fish taken
during late winter (February) had eggs that were
smaller (50.25 mm diameter) and fewer in number
(4060), while in April to May eggs were larger
(41.0 mm) and more numerous (up to 75 total).
Outcrossing, in which males presumably fertilize infertile eggs laid by hermaphrodites, is documented to
occur frequently in some locales in Belize, and with less
frequency in other populations (Lubinski et al. 1995;
Mackiewicz et al. 2006b). Except for the offshore cays
of Belize, males are rare, but even in populations in
which males are very rare or unknown, a certain

733

734

northerly latitudes (Richards et al. 2011). In fact, a

wide-ranging examination of the meristics/morphometrics of 12 populations ranging from Florida to
Honduras, and including two populations from
Brazil, documented a marginal increase in size at
more southerly latitudes (Taylor 2003).

Age and growth

Conclusion
Kryptolebias marmoratus, with its unique physiological attributes and bizarre reproductive/mating
system, has long been a source of fascination as a
laboratory organism and genetic model, and it is in
the forefront of research in these areas. However,
insights into its natural history and ecology have
not come easily, as this animal lives in a complex,
multi-dimensional, cryptic habitat that is widely
variable in its environmental and physical features.
We can now characterize the types of microhabitats
in which the mangrove rivulus might be found in the
field, and with this knowledge dedicated field biologists may now began to unravel more of its elusive
life in the wild.

Acknowledgment
William P. Davis and Bruce J. Turner have provided
years of inspiration in pursuit of this daunting
creature.

Funding
This work was supported in part by a NIH Conference
Grant R13HD070622 from the Eunice Kennedy
Shriver National Institute of Child Health & Human
Development; Society for Integrative and Comparative
Biology through the Division of Comparative
Endocrinology, Division of Comparative Physiology
and Biochemistry, Division of Animal Behavior
and the C. Ladd Prosser Fund; and the College of
Agriculture and Natural Resources, University of
Maryland. Field work in Belize was supported in part
by the Smithsonian Institution, Caribbean Coral Reef
Ecosystems Program.

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D. S. Taylor